Tuning adenosine A1 and A2A receptors activation mediates l-citrulline-induced inhibition of [3H]-acetylcholine release depending on nerve stimulation pattern

Neurochemistry International

Volumn 52, Issue 4-5, 2008, Pages 834-845

  Timoteo M A ^a   Oliveira, L ^a   Campesatto Mella, E ^b,c   Barroso, A ^a   Silva, C ^a   Magalhaes Cardoso M T ^a   Alves do Prado, W ^b   Correia de Sa P ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b STATE UNIVERSITY OF MARINGÁ   (Brazil)

^c Centro Universitario de Maringa   (Brazil)

Author keywords

Acetylcholine release; Adenosine; l Citrulline; Muscarinic M2 receptor; Neuromuscular junction; Nitric oxide

Indexed keywords

3 MORPHOLINYLSYDNONEIMINE; 4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ACETYLCHOLINE; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE DEAMINASE; ARGININE; CITRULLINE; IMIDE; MUSCARINIC M2 RECEPTOR; N(G) NITROARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROBENZYLTHIOINOSINE; OTENZEPAD; UNCLASSIFIED DRUG; 3 MORPHOLINO SYDNONIMINE; 3-MORPHOLINO-SYDNONIMINE; DRUG DERIVATIVE; ENZYME INHIBITOR; HEMOGLOBIN; MOLSIDOMINE; NEURONAL NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG BLOOD LEVEL; DRUG INHIBITION; FEMALE; HEMIDIAPHRAGM; MALE; NERVE STIMULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOSIDE TRANSPORT; PHRENIC NERVE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RAT; ANIMAL; DRUG EFFECT; ELECTROSTIMULATION; METABOLISM; MOTONEURON; NERVE ENDING; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYNAPTOSOME; WISTAR RAT;

RATTUS;

ACETYLCHOLINE; ADENOSINE; ANIMALS; ARGININE; CITRULLINE; ELECTRIC STIMULATION; ENZYME INHIBITORS; FEMALE; HEMOGLOBINS; MALE; MOLSIDOMINE; MOTOR ENDPLATE; MOTOR NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2A; SIGNAL TRANSDUCTION;

EID: 38349143952     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2007.09.016     Document Type: Article

References (60)

1. Baranano D.E., Ferris C.D., and Snyder S.H. Atypical neural messengers. Trends Neurosci. 24 (2001) 99-106
2. 1 receptors on motor nerve terminals. J. Neurochem. 94 Suppl. 2 (2005) 61
3. Blottner D., and Luck G. Just in time and place: NOS/NO system assembly in neuromuscular junction formation. Microsc. Res. Tech. 55 (2001) 171-180
4. 1 receptors protects NO-triggered rebound potentiation and LTP in rat hippocampal slices. J. Neurophysiol. 87 (2002) 1781-1798
5. Boulton C.L., Irving A.J., Southam E., Potier B., Garthwaite J., and Collingridge G.L. The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur. J. Neurosci. 6 (1994) 1528-1535
6. Broad R.M., Fallahi N., and Fredholm B.B. Nitric oxide interacts with oxygen free radicals to evoke the release of adenosine and adenine nucleotides from rat hippocampal slices. J. Auton. Nerv. Syst. 81 (2000) 82-86
7. Broome M.R., Collingridge G.L., and Irving A.J. Activation of NO-cGMP signalling depresses hippocampal synaptic transmission through an adenosine receptor-dependent mechanism. Neuropharmacology 33 (1994) 1511-1513
8. Chicoine L.G., Paffett M.L., Young T.L., and Nelin L.D. Arginase inhibition increase nitric oxide production in bovine pulmonary arterial endothelial cells. Am. J. Physiol. (Lung Cell Mol. Physiol.) 287 (2004) L60-L68
9. 2A-adenosine receptor of the rat motor nerve endings is positively coupled to adenylate cyclase. Naunyn-Schmiedeberg's Arch. Pharmacol. 350 (1994) 514-522
10. 3H]acetylcholine release from the rat motor nerve terminals. Neuroscience 73 (1996) 85-92
11. 2A adenosine receptor facilitation of neuromuscular transmission: influence of stimulus paradigm on calcium mobilization. J. Neurochem. 74 (2000) 2462-2469
12. 3H]acetylcholine release from the rat motor-nerve endings. Eur. J. Pharmacol. 406 (2000) 355-362
13. 2A facilitatory adenosine receptor activation balance depends on motor nerve stimulation paradigm at the rat hemidiaphragm. J. Neurophysiol. 76 (1996) 3910-3919
14. Cunha R.A. Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem. Int. 38 (2001) 107-125
15. Cunha R.A., Correia-de-Sá p., Sebastião A.M., and Ribeiro J.A. Preferential activation of excitatory adenosine receptors at the rat hippocampal and neuromuscular synapses by adenosine formed from released adenine nucleotides. Br. J. Pharmacol. 119 (1996) 253-260
16. Cunha R.A., and Sebastião A.M. Extracellular metabolism of adenine nucleotides and adenosine in the innervated skeletal muscle of the frog. Eur. J. Pharmacol. 197 (1991) 83-92
17. Curis E., Nicolis I., Moinard C., Osowska S., Zerrouk N., Bénazeth S., and Cynober L. Amost all about citrulline in mammals. Amino Acids 29 (2005) 177-205
18. Descarries L.M., Cai S., Robitaille R., Josephson E.M., and Morest D.K. Localization and characterization of nitric oxide synthase at the frog neuromuscular junction. J. Neurocytol. 27 (1998) 829-840
19. Fallahi N., Broad R.M., Jin S., and Fredholm B.B. Release of adenosine from rat hippocampal slices by nitric oxide. J. Neurochem. 67 (1996) 186-193
20. Faria M., Oliveira L., Timóteo M.A., Lobo M.G., and Correia-de-Sá P. Blockade of neuronal facilitatory nicotinic receptors containing alpha 3 beta 2 subunits contribute to tetanic fade in the rat isolated diaphragm. Synapse 49 (2003) 77-88
21. G-methylarginine requires NADPH-dependent hydroxylation. J. Med. Chem. 36 (1993) 491-496
22. Garthwaite J., and Boulton C.L. Nitric oxide signalling in the central nervous system. Annu. Rev. Physiol. 57 (1995) 683-706
23. Garthwaite J. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14 (1991) 60-67
24. Gustafsson L.E., Wiklund C.U., Wiklund N.P., Persson M.G., and Moncada S. Modulation of autonomic neuroefector transmission by nitiric oxide in guinea pig ileum. Biophys. Res. Comm. 173 (1990) 106-110
25. Hakim T.S., Sugimori K., Camporesi E.M., and Anderson G. Half-life of nitric oxide in aqueous solutions with and without haemoglobin. Physiol. Meas. 17 (1996) 267-277
26. Ignarro L.J. Signal transduction mechanisms involving nitric oxide. Biochem. Pharmacol. 41 (1991) 485-490
27. Katz B., and Miledi R. Transmitter leakage from motor nerve endings. Proc. R. Soc. Lond. B Biol. Sci. 169 (1977) 59-72
28. Lloyd H.G., and Fredholm B.B. Involvement of adenosine deaminase and adenosine kinase in regulating extracellular adenosine concentration in rat hippocampal slices. Neurochem. Int. 26 (1995) 387-395
29. 2A receptor facilitation of acetylcholine release at rat motor nerve endings. J. Physiol. (Lond.) 549.2 (2003) 399-408
30. Molenaar P.C., Oen B.S., Polak R.L., and van der Laaken A.L. Surplus acetylcholine and acetylcholine release in the rat diaphragm. J. Physiol. (Lond.) 385 (1987) 147-167
31. Moncada S., and Higgs A. The l-arginine-nitric oxide pathway. N. Engl. J. Med. 329 (1993) 2002-2012
32. Moncada S., Palmer R.M.J., and Higgs A. Nitiric oxide: physiology, pathophysiology and pharmacology. Pharm. Rev. 43 (1991) 109-142
33. Mori M., and Gotoh T. Regulation of nitric oxide production by arginine metabolic enzymes. Biochem. Biophys. Res. Commun. 275 (2000) 715-719
34. Morris Jr. S.M., Kepka-Lenhart D., and Chen L.C. Differential regulation of arginase and inducible nitric oxide synthase in murine macrophages cells. Am. J. Physiol. (Endocrinol. Metab.) 275 (1998) E740-E747
35. 1-purinoceptor-mediated inhibitory effects of adenosine and its stable analogues on the mouse hemidiaphragm preparation. Naunyn-Schmiedeberg's Arch. Pharmacol. 346 (1992) 197-202
36. Nickels T.J., Reed G.W., Drummond J.T., Blevins D.E., Lutz M.C., and Wilson D.F. Does nitric oxide modulate transmitter release at the mammalian neuromuscular junction?. Clin. Exp. Pharmacol. Physiol. 34 (2007) 318-326
37. Nikolsky E.E., Voronin V.A., Oranska T.L., and Vyskocil F. The dependence of non-quantal acetylcholine release on the choline-uptake system in the mouse diaphragm. Pflügers Arch. 418 (1991) 74-78
38. 1-receptor antagonist in live rats. Int. J. Neurosci. 115 (2005) 405-410
39. 1 receptors on rat motoneurons. NeuroSignals 14 (2005) 262-272
40. 3H]-acetylcholine release from the rat motor nerve terminals. Eur. J. Neurosci. 15 (2002) 1728-1736
41. 2+ influx into rat motor nerve terminals. J. Physiol. (Lond.) 560.1 (2004) 157-168
42. Paakkari I., and Lindsberg P. Nitric oxide in the central nervous system. Ann. Med. 27 (1995) 369-377
43. Parkinson S.J., Jovanovic A., Jovanovic S., Wagner F., Terzic A., and Waldman S.A. Regulation of nitric oxide-responsive recombinant soluble guanylyl cyclase by calcium. Biochemistry 38 (1999) 6441-6448
44. Ribera J., Marsal J., Casanovas A., Hukkanen M., Tarabal O., and Esquerda J.E. Nitric oxide synthase in rat neuromuscular junctions and in nerve terminals of Torpedo electric organ: Its role as regulator of acetylcholine release. J. Neurosci. Res. 51 (1998) 90-102
45. Rochon D., Rousse I., and Robitaille R. Synapse-glia interactions at the mammalian neuromuscular junction. J. Neurosci. 21 (2001) 3819-3829
46. Rosenberg P.A., Ya L., Le M., and Zhang Y. Nitric oxide-stimulated increase in extracelular adenosine accumulation in rat forebrain neurons in culture is associated with ATP hydrolysis and inhibition of adenosine kinase activity. J. Neurosci. 20 (2000) 6294-6301
47. Roszek B., Baan G.C., and Huijing P.A. Decreasing stimulation frequency-dependent length-force characteristics of rat muscle. J. Appl. Physiol. 77 (1994) 2115-2124
48. Rothe F., Langnaese K., and Wolf G. New aspects of the location of neuronal nitric oxide synthase in the skeletal muscle: a light and electron microscopic study. Nitric Oxide 13 (2005) 21-35
49. Ruiz E., and Tejerina T. Relaxant effects of l-citrulline in rabbit vascular smoth muscle. Br. J. Pharmacol. 125 (1998) 186-192
50. Silinsky E.M. On the association between transmitter secretion and the release of adenine nucleotides from mammalian motor nerve terminals. J. Physiol. (Lond.) 247 (1975) 145-162
51. Silinsky E.M. Adenosine decreases both presynaptic calcium currents and neurotransmitter release at the mouse neuromuscular junction. J. Physiol. (Lond.) 558 2 (2004) 389-401
52. Silinsky E.M. Modulation of calcium currents is eliminated after cleavage of a strategic component of the mammalian secretory apparatus. J. Physiol. (Lond.) 566 3 (2005) 681-688
53. Silva H.M.V., Ambiel C.R., and Alves-do-Prado W. The neuromuscular transmission fade (Wedensky inhibition) induced by l-arginine in neuromuscular preparations from rats. Gen. Pharmacol. 32 (1999) 705-712
54. Stamler J.S., and Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol. Rev. 81 (2001) 209-237
55. Thomas S., and Robitaille R. Differential frequency dependent regulation of transmitter release by endogenous nitric oxide at the amphibian neuromuscular junction. J. Neurosci. 21 (2001) 1087-1095
56. Wang T., Xie Z., and Lu B. Nitric oxide mediates activity dependent synaptic suppression at developing neuromuscular synapses. Nature 374 (1995) 262-266
57. 3H]-acetylcholine from a modified rat phrenic nerve-hemidiaphragm preparation. Naunyn-Schmiedeberg's Arch. Pharmacol. 334 (1986) 357-364
58. Wiklund C.U., Wiklund N.P., and Gustafsson L.E. Modulation of neuroefector transmission by endogenous nitiric oxide: a role for acetylcholine receptor-activated nictric oxide formation, as indicated by measurements of nitric oxide/nitrite release. Eur. J. Pharmacol. 240 (1993) 235-242
59. Wu G., and Morris Jr. S.M. Arginine metabolism: nitric oxide and beyond. Biochem. J. 336 (1998) 1-17
60. Yang C.C., Alvarez R.B., Engel W.K., Haun C.K., and Askanas V. Immunolocalization of nitric oxide synthases at the postsynaptic domain of human and rat neuromuscular junctions-light and electron microscopic studies. Exp. Neurol. 148 (1997) 34-44